Diverse interneuron populations have highly specific interconnectivity in the rat piriform cortex

Journal of Comparative Neurology

Volumn 518, Issue 9, 2010, Pages 1570-1588

  Gavrilovici, Cezar ^a   D'Alfonso, Sabrina ^a   Poulter, Michael O ^a  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Calcium binding protein; Epilepsy; Innervation; Interneuron; Piriform; Rat

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL JUNCTION; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC CELL; IMAGE ANALYSIS; IMMUNOREACTIVITY; INNERVATION; INTERNEURON; NERVE CELL PLASTICITY; NERVE ENDING; NEUROCHEMISTRY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRIFORM CORTEX; RAT;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CEREBRAL CORTEX; INTERNEURONS; MALE; NEURAL PATHWAYS; PARVALBUMINS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 77949386225     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22291     Document Type: Article

References (64)

1. Ballain T, Litaudon P, Martiel JL, Cattarelli M. 1998. Role of the net architecture in piriform cortex activity: analysis by a mathematical model. Biol Cybern 79:323-336.
2. Borden LA. 1996. GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem Int 29:335-356.
3. Chalazonitis A, Pham TD, Li Z, Roman D, Guha U, Gomes W, Kan L, Kessler JA, Gershon MD. 2008. Bone morphogenetic protein regulation of enteric neuronal phenotypic diversity: relationship to timing of cell cycle exit. J Comp Neurol 509:474-492.
4. Cossart R, Dinocourt C, Hirsch JC, Merchan-Perez A, De Felipe J, Ben Ari Y, Esclapez M, Bernard C. 2001. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 4:52- 62.
5. Cossart R, Bernard C, Ben Ari Y. 2005. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci 28:108-115.
6. Curtis MA, Penney EB, Pearson AG, Roon-Mom WM, Butterworth NJ, Dragunow M, Connor B, Faull RL. 2003. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci U S A 100:9023-9027.
7. De Biasi S, Vitellaro-Zuccarello L, Brecha NC. 1998. Immunoreactivity for the GABA transporter-1 and GABA transporter-3 is restricted to astrocytes in the rat thalamus. A light and electron-microscopic immunolocalization. Neuroscience 83: 815-828.
8. Dinocourt C, Petanjek Z, Freund TF, Ben Ari Y, Esclapez M. 2003. Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J Comp Neurol 459: 407-425.
9. Ekstrand JJ, Domroese ME, Feig SL, Illig KR, Haberly LB. 2001a. Immunocytochemical analysis of basket cells in rat piriform cortex. J Comp Neurol 434:308-328.
10. Ekstrand JJ, Domroese ME, Johnson DM, Feig SL, Knodel SM, Behan M, Haberly LB. 2001b. A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy. J Comp Neurol 434:289-307.
11. Ferraguti F, Cobden P, Pollard M, Cope D, Shigemoto R, Watanabe M, Somogyi P. 2004. Immunolocalization of metabotropic glutamate receptor 1alpha (mGluR1alpha) in distinct classes of interneuron in the CA1 region of the rat hippocampus. Hippocampus 14:193-215.
12. Freund TF. 2003. Interneuron Diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-495.
13. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
14. Fritschy JM, Weinmann O, Wenzel A, Benke D. 1998. Synapsespecific localization of NMDA and GABAA receptor subunits revealed by antigen-retrieval immunohistochemistry. J Comp Neurol 390:194-210.
15. Fritschy JM, Kiener T, Bouilleret V, Loup F. 1999. GABAergic neurons and GABAA-receptors in temporal lobe epilepsy. Neurochem Int 34:435-445.
16. Gavrilovici C, D'Alfonso S, Dann M, Poulter MO. 2006. Kindling-induced alterations in GABAA receptor mediated inhibition and neurosteroid activity in the piriform cortex of rat. Eur J Neurosci 24:1373-1384.
17. Gulyas AI, Hajos N, Freund TF. 1996. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16:3397-3411.
18. Haberly LB. 1983. Structure of the piriform cortex of the opossum. I. Description of neuron types with Golgi methods. J Comp Neurol 213:163-187.
19. Haberly LB. 2001. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26:551-576.
20. Haberly LB, Bower JM. 1984. Analysis of association fiber system in piriform cortex with intracellular recording and staining techniques. J Neurophysiol 51:90 -112.
21. Haberly LB, Sutula TP. 1992. Neuronal processes that underlie expression of kindled epileptiform events in the piriform cortex in vivo. J Neurosci 12:2211-2224.
22. Hutcheon B, Brown LA, Poulter MO. 2000. Digital analysis of light microscope immunofluorescence: high-resolution colocalization of synaptic proteins in cultured neurons. J Neurosci Methods 96:1-9.
23. Hutcheon B, Fritschy JM, Poulter MO. 2004. Organization of GABA receptor alpha-subunit clustering in the developing rat neocortex and hippocampus. Eur J Neurosci 19:2475-2487.
24. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA. 2001. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci U S A 98:4710-4715.
25. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, Greenberg DA. 2004. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 101:343-347.
26. A receptor beta 1-3 subunit gene expression in the hippocampus of kindled rats. Neurosci Lett 174:5-8.
27. Kanter ED, Kapur A, Haberly LB. 1996. A dendritic GABAA-mediated IPSP regulates facilitation of NMDA-mediated responses to burst stimulation of afferent fibers in piriform cortex. J Neurosci 16:307-312.
28. Kapur A, Pearce RA, Lytton WW, Haberly LB. 1997. GABAA-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J Neurophysiol 78:2531-2545.
29. Kawaguchi Y. 1993. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69:416-431.
30. Kawaguchi Y. 1995. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655.
31. Kawaguchi Y, Kondo S. 2002. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31: 277-287.
32. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
33. Kelly ME, Staines WA, McIntyre DC. 2002. Secondary generalization of hippocampal kindled seizures in rats: examining the role of the piriform cortex. Brain Res 957:152-161.
34. Kubota Y, Jones EG. 1993. Co-localization of two calcium binding proteins in GABA cells of rat piriform cortex. Brain Res 600: 339-344.
35. Kubota Y, Hattori R, Yui Y. 1994. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649:159-173.
36. Lehmann H, Ebert U, Loscher W. 1998. Amygdala-kindling induces a lasting reduction of GABA-immunoreactive neurons in a discrete area of the ipsilateral piriform cortex. Synapse 29: 299-309.
37. Loscher W, Ebert U. 1996. The role of the piriform cortex in kindling. Prog Neurobiol 50:427-481.
38. Luskin MB, Price JL. 1983. The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol 216: 264-291.
39. Magloczky Z, Freund TF. 2005. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci 28:334-340.
40. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
41. McBain CJ, Fisahn A. 2001. Interneurons unbound. Nat Rev Neurosci 2:11-23.
42. McIntyre DC, Wong RK. 1986. Cellular and synaptic properties of amygdala-kindled pyriform cortex in vitro. J Neurophysiol 55: 1295-1307.
43. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF. 1996. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
44. Minelli A, Brecha NC, Karschin C, DeBiasi S, Conti F. 1995. GAT-1, a high-affinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex. J Neurosci 15:7734-7746.
45. Miyata S, Nakai S, Kiyohara T, Hatton GI. 2000. Calbindin-D28k and calretinin in the rat posterior pituitary; light and electron microscopic localization and upregulation with dehydration. J Neurocytol 29:5-17.
46. Mody I. 2001. Distinguishing between GABAA receptors responsible for tonic and phasic conductances. Neurochem Res 26: 907-913.
47. Neville KR, Haberly LB. 2004. The synaptic organization of the brain. New York: Oxford University Press.
48. Nitsch R, Soriano E, Frotscher M. 1990. The parvalbumincontaining nonpyramidal neurons in the rat hippocampus. Anat Embryol 181:413-425.
49. Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC. 2007. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825-836.
50. Paxinos G, Watson PL. 1986. The rat brain in stereotaxic coordinates. Syndey: Academic Press.
51. BR1b receptors in the rat piriform cortex. Eur J Neurosci 12:1516-1520.
52. Racine RJ, Mosher M, Kairiss EW. 1988. The role of the pyriform cortex in the generation of interictal spikes in the kindled preparation. Brain Res 454:251-263.
53. Ribak CE, Tong WM, Brecha NC. 1996. GABA plasma membrane transporters, GAT-1 and GAT-3, display different distributions in the rat hippocampus. J Comp Neurol 367:595-606.
54. A receptors. Neuroscience 124:953-961.
55. Schnell SA, Staines WA, Wessendorf MW. 1999. Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47:719-730.
56. Sloviter RS. 1987. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73-76.
57. Somogyi J, Baude A, Omori Y, Shimizu H, El Mestikawy S, Fukaya M, Shigemoto R, Watanabe M, Somogyi P. 2004. GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat. Eur J Neurosci 19:552-569.
58. Stroemer RP, Kent TA, Hulsebosch CE. 1995. Neocortical neural sprouting, synaptogenesis, behavioral recovery after neocortical infarction in rats. Stroke 26:2135-2144.
59. Stroemer RP, Kent TA, Hulsebosch CE. 1998. Enhanced neocortical neural sprouting, synaptogenesis, and behavioral recovery with D-amphetamine therapy after neocortical infarction in rats. Stroke 29:2381-2393.
60. Suzuki N, Bekkers JM. 2007. Inhibitory interneurons in the piriform cortex. Clin Exp Pharmacol Physiol 34:1064-1069.
61. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H. 2002. Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12:395-410.
62. Whittington MA, Traub RD. 2003. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676-682.
63. Winsky L, Isaacs KR, Jacobowitz DM. 1996. Calretinin mRNA and immunoreactivity in the medullary reticular formation of the rat: colocalization with glutamate receptors. Brain Res 741:123-133.
64. Woo TU, Whitehead RE, Melchitzky DS, Lewis DA. 1998. A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia. Proc Natl Acad Sci U S A 95:5341-5346.